Tuberculosis in a South African prison – a transmission modelling analysis

Background. Prisons are
recognised internationally as institutions with very high tuberculosis
(TB) burdens where transmission is predominantly determined by contact
between infectious and susceptible prisoners. A recent South African
court case described the conditions under which prisoners awaiting
trial were kept. With the use of these data, a mathematical model was
developed to explore the interactions between incarceration conditions
and TB control measures.

Methods. Cell dimensions,
cell occupancy, lock-up time, TB incidence and treatment delays were
derived from court evidence and judicial reports. Using the Wells-Riley
equation and probability analyses of contact between prisoners, we
estimated the current TB transmission probability within prison cells,
and estimated transmission probabilities of improved levels of case
finding in combination with implementation of national and
international minimum standards for incarceration.

Results.Levels
of overcrowding (230%) in communal cells and poor TB case finding
result in annual TB transmission risks of 90% per annum. Implementing
current national or international cell occupancy recommendations would
reduce TB transmission probabilities by 30% and 50%, respectively.
Improved passive case finding, modest ventilation increase or decreased
lock-up time would minimally impact on transmission if introduced
individually. However, active case finding together with implementation
of minimum national and international standards of incarceration could
reduce transmission by 50% and 94%, respectively.

Conclusions.Current
conditions of detention for awaiting-trial prisoners are highly
conducive for spread of drug-sensitive and drug-resistant TB.
Combinations of simple well-established scientific control measures
should be implemented urgently.

S Afr Med J 2011;101:809-813.

Prisons have high burdens of tuberculosis (TB) where overcrowding, lack of ventilation and poor prevention practices dramatically increase transmission risks of TB.1
The TB burden is exacerbated in sub-Saharan Africa by a high prevalence
of HIV infection among inmates, as TB is the most common opportunistic
infection among people living with HIV in Africa.6 A
high TB prevalence and poor control policies within prisons also create
potential breeding grounds for multidrug-resistant TB (MDR-TB).4 TB transmission within prisons can also significantly impact on the wider community.5

South Africa has the fourth highest global incarceration rate, with more than 165 000 prisoners in 237 operational prisons.7 There is a rapid turnover of awaiting-trial prisoners with 79% being incarcerated for periods of less than 12 months.8 The number of individuals passing through the prison system annually therefore exceeds 368 000.8 Detainees
either awaiting sentencing or awaiting trial comprise approximately a
third of prisoners; they suffer the worst prison conditions, frequently
being kept in large crowded communal cells housing 40 - 60 inmates for
23 hours per day.7 International agencies recommend a minimum allocation of 5.4 m2 of floor space per prison inmate,11 while South African prison regulations stipulate a minimum allocation of 3.34 m2 floor area in communal cells.7
However, awaiting-trial prisoners are frequently housed in overcrowded
communal cells for prolonged periods of time with floor space
allocations as low as 1.4 m2 per inmate.7

South African prisons’ TB
notifications have not been reported in the public domain or included
in the annual judicial prison inspectorate reports.7
The consequences of overcrowding on TB transmission in prisons have
therefore not previously been quantified. However, previous
incarceration was found to be a significant risk factor for prevalent
TB in a population survey in Cape Town.12
Prison inmates elsewhere have been identified as at high risk for TB,
including MDR-TB and extensively drug-resistant TB (XDR-TB).4

A judgment was published in the case of Dudley Lee and the Minister
of Correctional Services in which the plaintiff developed TB while an
awaiting-trial prisoner in Pollsmoor prison, Cape Town.13
Evidence during the trial described an understaffed and poorly
functioning prison TB control programme, and data were presented on TB
incidence, delays in accessing TB diagnosis and care, hours of lock-up,
crowding and poor ventilation.

We aimed to explore probabilities of TB transmission of
awaiting-trial prisoners incarcerated in communal cells in Pollsmoor
correctional facility, Cape Town. We used the court case evidence13 as parameters in a deterministic model14,15 of the risks of TB transmission during imprisonment.

MethodsStudy design

TB transmission probabilities were estimated using the Wells-Riley
equation, a well-known transmission model that has been applied to a
wide range of transmission scenarios,14 including
describing airborne transmission probabilities within a single enclosed
room or space with defined ventilation characteristics.15
We used this equation in combination with the distribution of inmates
per cell and their probability of having TB that had been infectious
for different periods of time, in order to explore prisoner-to-prisoner
TB transmission probabilities. The modelled transmission probabilities
were adjusted for daily lock-up periods and variable cell ventilation
characteristics.

We then explored the effects of decreased crowding, shorter lock-up
times, improved ventilation and improved case finding on TB
transmission probabilities. Finally we explored combinations of changes
to the TB control programme and prison conditions necessary to achieve
significant reductions in TB transmission. Table I shows the values and
ranges of key parameters used to populate the model.

Prison population

Pollsmoor maximum-security prison is the
third-largest facility housing unsentenced prisoners in South Africa,
with approximately 3 200 awaiting-trial and unsentenced prisoners at
any time. They are predominantly incarcerated in communal cells of 40 -
60 prisoners and confined for 23 hours each day.13 Overcrowding is persistently high with reported average occupancy rates of 235% in 200313 and 239% in 2008.7 Cell ventilation is poor with a single slatted window on an exterior wall with openings of 6 088 cm2 and a small ventilator grille with area of 126 cm2 on the solid metal door, which is closed at night.

The TB control programme

South African prisons’ TB control programme is
similar to the national TB programme, which focuses on passive case
finding of sputum smear-positive cases and directly observed
short-course therapy.25
However, because of chronic nursing shortages the strategy was poorly
implemented, with no active case finding, and inmates with symptomatic
TB could wait up to 4 months before referral to the prison hospital.13 Medical staff did not systematically screen newly arriving prisoners for symptoms or signs of TB.13
Notification registers between 1998 and 2009 were inconsistently
completed, resulting in significant under-reporting of TB cases; 177
prisoners commenced TB therapy in 2001 – a notification rate of
5.5 TB cases per 100-person prison years.13
However, a prison medical officer gave evidence that during the year,
264 prisoners had laboratory confirmation of acid-fast bacilli on
direct sputum smear, indicating marked under-reporting of a TB
incidence rate of 8.25 cases per 100-person prison years, that MDR-TB
was prevalent among inmates, and that a staff member had died from this
form of the disease.13

Mathematical transmission model

The number of TB infections (C) occurring in a prison
cell with susceptible prisoners (S) was assumed to be a function of the
number of infectious cases (I), their infectivity (q = quanta of
infectious particles produced per hour), time of exposure (t = time of
exposure in minutes), respiration rate (p = litres per hour), and
germ-free ventilation (Q = litres per hour) as given by Wells-Riley
equation C = S(1-e-Iptq/Q).
The prevalence (P) of infectious adults at any time is given by the
annual smear-positive incidence rate (M = per cent) and the period of
infectivity (Δ = days) as P = M/[365/Δ]. The risk of
contact with an infectious adult is given by the Poisson distribution
(λI/I!)e-λ, where λ = P*(A-1) is the expected number of infectious cases in a cell with ‘A = I + S’ adults.

Modelled input parameters

Germ-free ventilation (Q) was calculated as air
changes per hour (ACH) for a standard cell of 9.1 m long × 6.4 m
wide × 3.35 m high with a volume of 195 m3 .
Current cell ventilation would provide less than 1 ACH with all windows
and the door ventilator grille open with totally free flow of air
through the cell and a 10 km/h wind directed towards the window.26 International recommendations for prison ventilation22 based on the floor area of this cell would recommend
1.8 - 3.58 ACH, and the World Health Organization (WHO) recommends 12
ACH for health settings and congregate settings where TB is prevalent.23 Four values of ACH were therefore modelled: the status quo
of 1 ACH (poor ventilation); 3 ACH (minimum international recommended
ventilation); 8 ACH (intermediate ventilation); and 12 ACH (optimal
ventilation).

A wide range of estimated values for the rate of
production of infectious TB quanta (q) have been reported. Laryngeal TB
is highly infectious with ‘q’ estimated at 60 infectious
quanta per hour.16 In a
workplace outbreak due to an untreated smear-positive pulmonary case,
‘q’ was estimated at 12.7 infectious quanta per hour.18 Over a 2-year period in a TB ward, ‘q’ was directly measured at 1.25 infectious quanta per hour.15
A study applying molecular strain characterisation to track airborne TB
transmission from HIV/TB-infected inpatients to guinea pigs
demonstrated markedly variable infectiousness.27
Values of ‘q’ for infectious cases varied between 3 and 12
and 2.5 and 226 quanta per hour for individuals with drug-sensitive and
MDR-TB respectively. In order to be conservative, ‘q’ was
modelled at a mean value of 1 infectious quantum per hour.

The mean
respiratory rate of adults (p) was estimated to be 360 litres per hour
corresponding to a normal adult respiratory minute volume of 6 litres
per minute.24

A key parameter
of the model, the period of infectiousness (Δ), has a strong
inverse association with the TB control programme effectiveness of case
finding. Δ is a composite of delays, including time to access
medical care, diagnostic delay and time to commence chemotherapy. The
diagnostic delay period during which an adult may be infective is
variable, but is frequently reported to be 60 - 90 days.21
However, delays in accessing treatment within this prison were reported
to be very prolonged; therefore analyses were performed with values of
Δ from 1 day up to 180 days.

Passive case
finding depends on individuals with symptoms of TB self-presenting for
investigation. It was modelled that with increased TB awareness health
messaging, minimal delay in accessing TB services, expeditious
diagnosis and rapid initiation of chemotherapy, the period of
infectiousness (Δ) could be reduced to 60 days. Active case
finding (regular seeking out symptomatic prisoners) and rapid
diagnostic testing28 was modelled with values of Δ of less than 60 days.

Results

We explored the impact of cell occupancy on TB
transmission probabilities. Transmission probabilities at existing
levels of overcrowding, the recommended minimum South African and
international recommended occupancy are shown across a spectrum of time
periods of infectiousness of source cases (Δ) from 1 to 180 days
in Fig. 1. Transmission probabilities under prevailing conditions of
incarceration were estimated at 90% per annum for all values of Δ
(>60 days) currently implementable by the prison TB control
programme. The benefits of decreasing cell crowding were proportionate
at all values of Δ. Implementing current South African
recommended cell minimum levels of occupancy would reduce transmission
by 30% and implementing international recommendations would reduce
transmission by over 50%, even with current levels of TB case finding.

The effect of
decreasing lock-up time (period restricted to cells each day) is shown
for the existing conditions of 23 hours per day and for reductions to
12 and 8 hours per day respectively in Fig. 2. The benefits of
decreasing lock-up time are modest at current values of Δ
(approximately 180 days). However, the benefits of decreased lock-up
times are amplified by improving case finding with consequent
reductions in Δ. When Δ is reduced to 60 days, reduction of
lock-up time to 12 and 8 hours would reduce TB transmission by 10% and
20%, respectively.

The effect of
cell ventilation on TB transmission probability is shown in Fig. 3.
Three levels of ventilation were modelled in addition to the current
reported estimate of 1 ACH: 3 ACH; 8 ACH; and 12 ACH. Improved
ventilation markedly decreases TB transmission probabilities at all
values for Δ. However, improvements in ventilation are amplified
when accompanied by reductions in the value of Δ which could be
achieved by improved case finding.

Finally, we explored effects of improved case finding in three different scenarios (Fig. 4): scenario 1 – status quo;
scenario 2 – current South African regulations for imprisonment
with modest increase of ventilation to 3 ACH fully implemented; and
scenario 3 – international standards for imprisonment together
with ventilation at 12 ACH fully implemented. Improving passive case
finding to achieve a Δ of 60 days would have minimal effect on TB
transmission in scenario 1 and 20% and 50% reductions in scenarios 2
and 3, respectively. Active case finding to achieve a Δ of 30
days would decrease transmission by 10% with current scenario 1, 50%
with implementation of scenario 2, and 90% with implementation of
scenario 3.

Discussion

This study shows that conditions prevailing in a
South African prison are extremely conducive for ongoing transmission
of TB. Crowding, substandard living conditions and a poorly functioning
prison TB control programme combine to contribute to high TB
transmission risks. Overcrowding of cells directly and proportionately
increases the probability of contact with infectious sources. Delays of
3 - 4 months in accessing medical care,13 together with time required for diagnosis and implementing therapy,21 markedly increase the prevalence of infectious cases, and act as the primary source for ongoing transmission.

We show that the
very high prevalence of infectious cases within the prison population
potentially negates the benefits of improved ventilation and shortened
exposure time within cells. The interdependence of all the transmission
risk factor parameters is further highlighted by the observation that
improved passive case finding sufficient to reduce the period of
infectiousness from 6 to 2 months would have a minimal effect under
current conditions of crowding and poor ventilation. However, the
multiplicative benefits of concurrent improvements in case finding,
crowding and environmental conditions are demonstrated. Active case
finding and implementing current national minimum standards of cell
occupancy7 can reduce transmission by 50%. Introducing international environmental standards22,23 could reduce transmission from the status quo by as much as94%.

Our study
strength was available accurate information specific to this prison:
number of TB cases, cell dimensions, number of prisoners per cell and
likely delays in accessing TB treatment. A limitation of the model is
that precise enumeration of the number of infective quanta produced by
a prisoner with TB is difficult. A very conservative estimate was
therefore derived from published data.15,25,26
The modelled analysis was also restricted to transmission events within
an illustrative typical communal prison cell within a single
operational prison. However, similar and even more severely crowded
conditions are endemic in South African prisons.7
The model was based on the epidemiological assumption that the TB
epidemic was generalised, with equal mixing of infectivity and contact
risks. Therefore the analysis was restricted to transmission events
occurring within the cell, and stochastic transmission events such as
close contact with highly infectious individuals outside the cell are
not captured. Despite these limitations, the model outputs are
compatible with the very high TB incidence rate relative to the rest of
Cape Town’s population,13,29 and robustly demonstrated the proportional impact of different control strategies on transmission probabilities.

The analysis was
restricted to acquisition of infection and not development of disease.
The relationship between newly acquired infection and disease
development is complex.30,31 Prior TB infection in immune-competent individuals, which is common in Cape Town,32 gives some protection against disease related to subsequent infection.33 However, those not previously infected,34 those with previously treated TB31 and those with HIV infection35
would be particularly vulnerable to progress to active TB disease
following recent exposure to infection. We did not specifically address
transmission of MDR- and XDR-TB, but transmission risks with these may
be heightened as a result of the prolonged period of infectiousness
that often results from failure of diagnosis and subsequent receipt of
inappropriate therapy. However, accurate MDR- and XDR-TB prevalence
data are not available to permit modelling.

‘A society should be judged not by how it treats its outstanding citizens but by how it treats its criminals.’36 We show that the conditions in which awaiting-trial prisoners are confined fall far below our own national7,13 and international standards for incarceration22,23
and constitute a health emergency. The medical and environmental health
professions and the judiciary must urgently work with the Department of
Correctional Services to institute simple scientifically based disease
control measures that need to be tailored to circumstances and
resources. Many strategies are available to address the problem. The
Judicial Inspectorate has repeatedly proposed the measures required to
decrease the awaiting-trial prison population.7
Cell ventilator grills should not be closed at night; cross-ventilation
of communal cells could be encouraged by using barred rather than solid
doors and incorporating corridor ventilator extraction systems. Since
1847, carbon dioxide levels have been used as a measure of adequate
ventilation37
and carbon dioxide monitoring could readily establish if effective
improvements in cell ventilation are being achieved. Prison TB control
programmes should introduce active case finding21 and use recent technological advances in rapid TB diagnosis and drug resistance.28
TB notification data for South African prisons should not be considered
secret or restricted information, but accurate data should be made
available to the Judicial Inspectorate of Prisons to include in the
annual report on the state of our prisons.7

TB transmission
risks within our prison system are unacceptably high, posing a direct
hazard to prisoners and contributing to the general population TB
burden. Overlooking TB prevention and control in prisons carries
serious health consequences for both prisoners and the general
community.1,38

37. De Chaumont F.
On the theory of ventilation: an attempt to establish a positive basis
for the calculation of the amount of fresh air required for an
inhabited air-space. Proc R Soc Lond 1874;23:187-201.

37. De Chaumont F.
On the theory of ventilation: an attempt to establish a positive basis
for the calculation of the amount of fresh air required for an
inhabited air-space. Proc R Soc Lond 1874;23:187-201.

Desmond Tutu HIV Centre, Institute of Infectious
Diseases and Molecular Medicine, University of Cape Town, and
Department of Clinical Research Unit, Faculty of Infectious and
Tropical Diseases, London School of Hygiene and Tropical Medicine,
London, UK

Stephen D Lawn, BMedSci, MB BS, MRCP (UK), MD, DTM&H, Dip HIV Med

DST/NRF Centre of Excellence in Epidemiological Modelling and Analysis, Stellenbosch University

Alex Welte, PhD

Desmond Tutu HIV Centre, Institute of Infectious
Diseases and Molecular Medicine, and Department of Medicine, University
of Cape Town

Linda-Gail Bekker, MB BS, FCP (SA), PhD

Desmond Tutu HIV Centre, Institute of Infectious
Diseases and Molecular Medicine, University of Cape Town, DST/NRF
Centre of Excellence in Epidemiological Modelling and Analysis,
Stellenbosch University, and Department of Medicine, University of Cape
Town

NB *TB incidence rate based on 177 cases in prison population of 3 200.13

†ACH = air changes per hour for cell of 195 m3 volume.

‡ Cell floor area is 9.1 m × 6.4 m = 58.24 m2 . Prisoners per cell = the floor area divided by the space allocated per prisoner, a minimum of 3.34 m2 according to South African regulations. If the cell was 200% full then there would be twice as many prisoners present.

Fig. 1. The effect of prison cell overcrowding on
TB transmission probabilities is plotted against time periods of
infectiousness up to 180 days. They are shown for 3 levels of
overcrowding; 250% approximates the current level cell occupancy;13 100% represents implementation of current South African statutory minimum occupancy of 3.44 m2 of floor space per inmate,7 and 50% corresponds to international space recommendations.22

Fig. 2. The effect of length of period of
restriction in prison cell per day on TB transmission probabilities is
plotted against time periods of infectiousness up to 180 days, shown
for 3 time periods of cell occupancy during a 24-hour period; 23
hours per day, 12 hours per day and 8 hours per day. NB: 23 hours per
day is the current period of restriction to cells in Pollsmoor prison.13

Fig. 3. The effect of increasing levels of cell
ventilation on TB transmission probabilities is plotted against time
periods of infectiousness up to 180 days. They are shown for 4 values
of ventilation air change per hour (ACH): 1 ACH (current estimated cell
ventilation), 3 ACH (minimal international recommendation),22
8 ACH (moderately increased ventilation) and 12 ACH (the optimal level
of ventilation recommended by WHO for health care settings).23